Breath hydrogen excretion after oral administration of xylose to cats

Breath hydrogen excretion after oral administration of xylose to cats P. Muir*, T. J. GruEydd-Jones, P. J. Cripps, K. Papasouliotis and P. J. Brownt

The Feline Centre, Department of Veterinary Medicine, and tThe Comparative Pathology Laboratory, Department of Vet- erinary Pathology and Microbiology, University of Bristol, Langford, Bristol BS18 7DU

Journal of Small Animal Practice (1994) 35, 86-92

ABSTRACT Maximum breath hydrogen excretion after the

oral administration of xylose to 11 healthy cats ranged from 0.13 ml/hour to 0.47 ml/hour, with a mean of 0.18 ml/hour. After oral administration of xylose, breath hydrogen excretion in five cats with chronic diarrhoea and, or, vomiting was significantly different (P<0.001) compared with healthy cats. Increased breath hydrogen excretion occurred before xylose was given and at all measurement times after its administration to the sick cats (P<0.05), indicating carbohydrate malassimilation. In four sick cats, large increases in breath hydrogen excretion occurred, with maximum values ranging from 1.21 to 1.56 ml/hour, but in one cat the maximum value was only 0.28 ml/hour. Plasma xylose concentrations in cats with chronic diarrhoea and, or, vomiting were not significantly different from healthy cats (P>0.05) and thus did not demonstrate carbohydrate malassimilation. A hiatus hernia was seen on radiographic views of the thorax and abdomen of one cat with chronic vomiting. Inflammatory bowel disease was found in three of the five sick cats after upper gastrointestinal endoscopic examination and mucosal biopsy. Clostridium species were isolated in increased

* Dr Muir's current address is The University of Wisconsin- Madison, School of Veterinary Medicine, Department of Sur- gical Sciences, Madison, Wisconsin 53706, USA

numbers from the cats with chronic diarrhoea and, or, vomiting (P<0.005), after quantitative bacterial culture of small intestinal fluid specimens obtained endoscopically. Clostridium species were isolated from all five cats with chronic diarrhoea and, or, vomiting but from only one of eight healthy cats. However, whether a specific bacterial pathogen caused the increased breath hydrogen excretion found in these cats could not be determined'from this study.

INTRODUCTION Chronic intestinal disease, particularly inflam-

matory bowel disease, is becoming increasingly recognised as an important cause of diarrhoea, vomiting and weight loss in cats (Dennis and others 1992). However, many diagnostic tests for malassimilation in dogs (Jacobs and others 1989) have not yet been applied to cats (Nicholson and others 1989). Measurement of breath hydrogen excretion is commonly used to diagnose carbohydrate malassimilation in humans (Perman 1991) and this technique has been applied to dogs (Washabau and others 1986a) and cats (Muir and others 1991). It can also detect carbohydrate malassimilation in these species (Washabau and others 1986a,b, Muir and others 1991).

This study reports the results from five cats with chronic diarrhoea and, or, vomiting, in which measurement of breath hydrogen excretion and plasma xylose absorption was performed simultaneously because of suspected malassimilation. Xylose absorption in healthy cats is variable (Sherding and others 1982) and significant differences in xylose absorption have not been detected by measurement of plasma xylose absorption in cats with infiltrative intestinal disease (Hawkins and others 1986).

MATERIALS AND METHODS Animals

Eleven healthy cats (1 to 11) of both genders, aged between one and 15 years, were used. They ranged in weight from 2.7 to 5.8 kg and were deemed to be healthy on the basis of physical examination and previous history.

Over a six-month period, five cats (A to E), were referred by veterinarians to the Feline Cen- tre at the University of Bristol, School of Veteri- nary Science, for further investigation of chronic diarrhoea and, or, vomiting and weight loss. At presentation, the relevant history was recorded, a physical examination was performed and each cat was hospitalised. Cats A to D had chronic

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Breath hydrogen excretion after oral administration of xylose to cats

diarrhoea, with a pattern indicative of abnormal- ity of the small intestine. Cat E was presented principally for chronic vomiting; cats A and D also vomited intermittently. All cats had moder- ate to severe weight loss. Cat D was also pruritic, with areas of alopecia and hyperkeratosis. The cats ranged in age from one to seven years, and weighed from 1-7 to 4.0 kg. The age of cat B was unknown.

Routine diagnostic investigations

Blood samples were collected and examined haematologically (cats A to E) and biochemically (cats A to E) and tested for feline leukaemia virus and antibodies to feline immunodeficiency virus (cats A, C and D). Faecal samples were collected from cats A to D. Selective media plates were inoculated with faecal specimens to attempt iso- lation of Campylobacter species, Salmonella species and Clostridium difficile (cats A to C). Saline flotation and a McMaster counting chamber were used to examine the faeces for parasite ova (cats A and D). A contrast radiographic study of the upper gastrointestinal tract of cat E was performed.

Breath hydrogen and plasma xylose absorption testing

Food was withheld overnight before the test. Breath hydrogen excretion was measured as pre- viously described (Muir and others 1991). Exhaled breath samples were collected using a semiclosed system. During sampling, the cats were confined in a plastic chamber. Holes were drilled around the base of the box to allow air to flow into the chamber. Air was continuously extracted from the top of the chamber by means of a pump with flow meter and a flow rate adjuster (MP5OW; Sibata Scientific Technology). The dilution of expired air was minimised. Air was passed from the outlet of the pump through a flow transducer connected to a portable respiratory air monitor (Portable Respiratory Air Moni- tor; Harvard Apparatus). The monitor measures the volume of extracted air and automatically collects part of the air into a plastic bag over a sampling period of five minutes.

Breath hydrogen excretion (ml/hour) was cal- culated from the volume of air recorded by the monitor; the sampling time was set on the monitor and the hydrogen concentration in duplicate air samples taken into a 20 ml plastic syringe from the collection bag. The concentration of hydrogen in the air samples was measured by a hydrogen monitor (GMI Exhaled Hydrogen Moni- tor; GMI Medical), with an electrochemical detector calibrated with a standard gas mixture.

Breath samples for hydrogen measurement were collected from all the cats every 15 minutes

for three hours after oral administration of 0.75 g/ kg xylose, diluted in water to 0.1 g xylose/ml. Blood samples for measurement of plasma xylose absorption were collected every 30 minutes from the time of xylose administration for two hours (cats 1 to 11 and A to D).

Upper gastrointestinal endoscopy, mucosal biopsy and intestinal fluid sampling

Before endoscopy, the instrument was disin- fected with a preparation containing formalin and succindialdehyde (Gigasept; Sterling Medi- care). Immediately before use, the endoscope instrument channel was flushed with sterile saline and then air. After food was withheld overnight, upper gastrointestinal endoscopy (Willard 1989, Guilford 1990) was performed under general anaesthesia, using a flexible fibre- optic gastroscope with a 9 mm insertion tube (Olympus Gastrointestinal Fibrescope P3 with a 100" forward viewing lens, Keymed). Gastric (cat E) and small intestinal mucosal biopsies (cats 4 to 11 and A to E) were collected. The biopsies from these cats were examined and reviewed by one individual (P.J.B.), after being processed by routine histopathological methods.

Small intestinal fluid specimens for quantitative bacterial culture were also collected with the endoscope after the method of Knutson and

'others (1982), using a sterile 1.8 mm diameter catheter (cats 4 to 11 and A to E). The tip of the endoscope was positioned 80 cm from the mouth for sampling. The catheter's lumen was filled with sterile saline and then it was passed several centimetres beyond the endoscope's tip. The saline in the catheter was aspirated and discarded. Because intestinal fluid could not usually be aspirated, 2 to 5 ml of sterile saline were intro- duced into the intestinal lumen and subsequent- ly aspirated, after the catheter had been flushed with a small bolus of air. The first part of the aspirate was discarded and the remainder was then placed in a sterile container and tightly sealed. The specimen was inoculated on to agar plates within 20 minutes of sampling. Through- out the procedure, the introduction of air into the gastrointestinal tract was minimised.

Specimens of sterile saline flushed through a sterile catheter placed through the endoscope, water from the reservoir bottle and water from the aidwater channel were obtained on five separate occasions, after only cleansing of the endoscope. Quantitative culture of these specimens was performed to estimate instrument contamination with bacteria.

Bacterial counts

Protozoa were not seen on direct microscopy of samples from all the small intestinal fluid

87

P. MUIR AND OTHERS

specimens collected. Media used for bacterial culture were blood agar, MacConkey agar, deMan Rogosa and Sharpe agar, fastidious anaerobe agar with and without gentamicin, and bile aesculin agar (Sutter and others 1980). A colony counting technique, based on methods described by Bin- gen and Lambert-Zechovsky (1984) and Sutter and others (1980), was used. Tenfold dilutions of the specimen from lo-' to lo-*, were prepared in an anaerobic cabinet using reduced 0.05 per cent yeast extract in normal saline. Plates intended to detect anaerobes were inoculated and incubated in an anaerobic cabinet. Plates intended to detect aerobes were inoculated in room air and incubated in a 5 per cent carbon dioxide atmosphere. The campylobacter plates were also inoculated in room air, but were incubated in a hydrogen and carbon dioxide atmosphere (Campypak; BBL Microbiology Systems). A drop (10 p1) of each dilution was spread on duplicated half-plates of media, using a sterile loop. Single whole plates of media were also inoculated with 10 pl of undiluted fluid, which was spread out to obtain individual colonies. Additionally, single whole plates of media were also inoculated for the iso- lation of C difficile, Bifidobacterium species (Sutter and others 1980) and Campylobacter species. All the plates incubated aerobically were examined a day later. The anaerobically incubated plates and the campylobacter plates were examined after two days. After appropriate incu- bation, colonies on the plates were counted and the species identified where possible, using standard techniques.

Water and saline specimens collected from the endoscope were centrifuged (Cytospin; Shandon Southern Products) and a Gram's stained smear of the sediment was examined microscopically. Single whole plates of blood agar and fastidious anaerobe agar without gentamicin were inoculated with 10 pl of undiluted fluid, incubated and examined as described above.

Data analysis Because the distribution of breath hydrogen

concentrations was approximately log normal, the readings were log transformed before analysis. Recorded zero values were recoded to the minimum concentration that the system could measure. Repeated measures analysis of variance was used to evaluate the effect of group (healthy or diseased) and time (after xylose administration) on breath hydrogen excretion and plasma xylose absorption. Significant differences were further evaluated with post hoc t tests. Bacterial counts were expressed as colony forming units (cfu)/ml. The Mann Whitney U test was used to compare the bacteriological data from healthy cats and cats with chronic diarrhoea and, or, vomiting after the counts were transformed to log

(n+l). Comparisons were considered significant at P<0.05, on a null hypothesis of no difference.

RESULTS Clinical and routine laboratory examinations

A hiatus hernia was identified in cat E radio- graphically. Leucocytosis and monocytosis were recorded in all the sick cats. Lymphocytosis was present in cat C and eosinophilia in cat D. Red blood cell and serum biochemical values were normal. No cat tested positive for feline leukaemia virus or antibodies to feline immunodeficiency virus. Salmonella species, Campy- lobacter species and C difficile were not isolated from faecal specimens and no parasite eggs were seen.

Breath hydrogen and plasma xylose tests

Mean breath hydrogen excretion in healthy cats before xylose administration was 0.10 ml/ hour (Fig l), with a range of <0.06 to 0.25 ml/ hour. Mean maximum breath hydrogen excretion after xylose administration to these cats was 0.18 ml/hour at 120 minutes (Fig l), with individual maximum values from 0-13 to 0.47 ml/hour and occurring at times varying from 0 to 180 minutes. Small increases in breath hydrogen excretion after xylose administration were detected in one healthy cat from 105 to 180 minutes.

After oral administration of xylose, breath hydrogen excretion in cats with chronic diarrhoea and, or, vomiting was significantly different (P<O-OOl) compared with healthy cats. Increased breath hydrogen excretion occurred before xylose was given and at all measurement times afterwards (P<0.05) (Fig 1). Within groups, the effect of time after xylose administration on

- - M l h y cats (n-1 l ) , fed 0.75 gkg xybse Cab wim Chmnic Diarrhoea and. or. Vomiting (n=5). fed 0.75 gkg wlose

0 30 Bo 90 120 150 180

Tlm Xylosa Admlnldraikn (rnlnuws)

FIG 1. Mean breath hydrogen concentrations after xylose administration. Error bars show the standard error of the mean

aa


- Healthy Cats (n-1 I ) , fed 0.75 gkg xylose - Cats with Chronic Diarrhoeaor Vomning (n-4), led 0.75 gkg xyloss

0 30 60 90 120

Tlme after Xyloaa Admlnlstratlon (mlnutes)

FIG 2. Mean plasma xylose concentrations after xylose administration. Error bars show the standard error of the mean

breath hydrogen excretion was not significant (P>0.05), nor was the interaction of group with time after xylose administration (P>0.05). In cats A to C and E, large increases occurred, with maximum values from 1.21 to 1.56 ml/hour, at times varying from 75 to 180 minutes after xylose administration. However, in cat D increases were small with a maximum of only 0.28 ml/ hour at 105 minutes. In this cat, breath hydrogen excretion exceeded mean values for healthy cats at all time points from 0 to 120 minutes after xylose administration.

After oral administration of xylose, plasma xylose absorption in cats with chronic diarrhoea and, or, vomiting was not significantly different (P>0.05) compared with healthy cats (Fig 2). In healthy cats, plasma xylose concentrations increased after xylose administration, and maximum values were reached at 60 minutes in five cats and at 90 minutes in two cats. In three cats, the highest recorded xylose concentration was at 120 minutes and in one cat, plasma xylose concentrations recorded at 60 and 90 minutes were

the same. Maximum concentrations varied from 2.6 to 6-3 mmol/litre. In the cats with chronic diarrhoea and, or, vomiting, a similar pattern of xylose absorption was seen. Plasma xylose concentrations reached a maximum at 60 minutes in one cat and at 90 minutes in two cats. In cat D, plasma xylose concentrations at 60 and 90 minutes were 3.9 mmol/litre. Maximum concentrations varied from 3.4 to 5-2 mmol/litre. Within groups, the effect of time after xylose administration on plasma xylose concentration was significant ( P < O - O O l ) . The interaction of group with time after xylose administration was not significant (P>0.05).

Endoscopic mucosal biopsy

Mucosal biopsies from the healthy cats were normal (Fig 3). The gastric biopsy from cat E was also normal. Inflammatory changes were found in the small intestinal mucosa of cats A, C and D. Infiltration by lymphocytes and plasma cells was found in cats A and C. Infiltration by mixed inflammatory cells was found in cat D (Fig 3). The small intestinal biopsies from cats B and E were normal.

Bacterial counts

Healthy cats. - The bacterial species or genera isolated are described in Table 1. Anaerobic counts did not exceed aerobic ones. The total number of bacteria isolated exceeded lofi cfu/ml in one specimen. Occasionally, aerobic counts exceeded lo5 cfu/ml and anaerobic ones exceeded lo4 cfu/ml (three of eight and two of eight specimens, respectively).

Cats with chronic diarrhoea and, or, vomiting. - The bacterial species or genera isolated are described in Table 2. Anaerobic counts exceeded aerobic bacteria in two specimens. The total number of bacteria isolated exceeded lo6 cfu/ml in two specimens. Aerobic counts exceeded

FIG 3 . Photomicrographs of small intestinal biopsies. (Left) Biopsy from a healthy cat with a normal villus for comparison. Haematoxylin and eosin x 200. [Right) Biopsy from cat D with infiltration of a villus with mixed inflammatory cells. Haema- toxylin and eosin X 150

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1 Table 1. Number and kind of bacteria isolated from proximal small intestinal fluid specimens obtained endoecopi- cally from healthy cats

* Undiluted specimen

l o5 cfu/ml in two specimens, and anaerobic counts exceeded lo4 cfu/ml in three specimens. Clostridium species were isolated in increased numbers from the cats with chronic diarrhoea and, or, vomiting compared with healthy cats (P<0.005). Differences in the number of bacteria isolated from the cats with chronic diarrhoea and, or, vomiting compared with healthy cats were not significant for total numbers of bacteria (P>0.05), total aerobic counts (P>0.05) and total anaerobic counts (P>0-05).

Endoscope contamination. - Small numbers of Bacillus species (lo2 cfu/ml in two of five specimens) and Pseudomonas species (lo2 cfu/ml in one of five specimens) were isolated from the water bottle. Bacillus species (lo2 cfu/ml in three of five specimens) and Pseudomonas species (4 x 10' cfu/ml in one of five specimens) were also isolated from the aidwater channel. A yeast (lo2 cfu/ml in one of five specimens) and Xan- thomonas maltophila ( lo2 cfu/ml in one of five specimens and >lo4 cfu/ml in one of five specimens) were isolated from the saline samples.

Table 2. Number and kind of bacteria isolated from proximal small intestinal fluid specimens obtained endoscopically from cats with chronic diarrhoea and, or, vomiting

* Undiluted specimen t Clostridiurn species were isolated in increased numbers

Carnpylobacter species were also isolated from the small compared with healthy cats (Pc0.005)

intestinal specimen of cat C

~ ~

DISCUSSION Although quantitative bacteriological examina-

tion of small intestinal fluid is the standard method for diagnosing small intestinal bacterial overgrowth and is regarded as more reliable than breath hydrogen testing in detecting this condi- tion (King and Toskes 1979, Corazza and others 1990), measurement of breath hydrogen excretion in cats may be a useful screening test for small intestinal bacterial overgrowth, as it is more diffi- cult to obtain small intestinal fluid aspirates from cats than humans. Breath hydrogen testing is quick and easy to perform, whereas quantitative bacterial culturing is more time consuming and expensive. In this study, measurement of breath hydrogen excretion both before and after oral administration of xylose demonstrated carbohydrate malassimilation in the sick cats, whereas the plasma xylose absorption test, which has been reported to be a poor test for intestinal disease in cats (Hawkins and others 1986), did not. The carbohydrate malassimilation is likely to be a consequence of intestinal disease, such as small intestinal bacterial overgrowth, as described in humans (Perman and others 1984, Corazza and others 1990). Why only small increases in breath hydrogen excretion were recorded in one of the five cats, which was affected with inflammatory bowel disease,'is unclear. The test may have been affected by factors such as alterations in the colonic flora (Gilat and others 1978).

90


Separate early peaks in breath hydrogen excretion after oral administration of lactulose have been considered a consequence of small intestinal bacterial overgrowth in humans (Rhodes and others 1979). In this study, separate small intestinal and colonic peaks were found, but time after xylose administration had no significant effect on breath hydrogen excretion. Therefore this pattern of breath hydrogen excretion may not reliably indicate small intestinal bacterial overgrowth in cats, as was also the case in a more recent human study (Corazza and others 1990). Carbohydrate fermentation by flora of the oral cavity may contribute to separate early peaks in breath hydrogen excretion after carbohydrate administration (Thompson and others 1986), but similar early peaks were not found in the healthy cats.

Collection of small intestinal fluid specimens by endoscopy has not been widely performed in cats. The routine cleansing technique used in this study did not always yield sterile saline specimens after saline was flushed through a catheter inserted through the instrument channel. Bacterial contamination of the aidwater channel was also present after cleansing. Although contaminants were not genera typically associated with small intestinal bacterial overgrowth, gas sterilisation is the preferred method of endoscope preparation for bacteriological studies (Knutson and others 1982, Willard 1989).

Many bacteria typical of oropharyngeal flora, such as Streptococcus, Pasteurella and Fusobac- terium species and which were isolated both from the healthy and the sick cats, may have been isolated from intestinal fluid specimens because contamination occurred during collection, Antiseptic preparation of the oropharynx before endoscopy, or use of a plugged double- sheathed aspiration catheter (Darien and others 1990) might reduce such contamination. How- ever, unguarded aspiration catheters were satis- factory for specimen collection for bacterial culture in humans (Rasmussen and others 1983, Corazza and others 1990).

Variations in patient and endoscope preparation, oropharyngeal contamination, saline sample dilution, preparation of media and their type, and media inoculation might all have affected the colony counts obtained. Although dilution of intestinal fluid during collection is undesirable, it may be necessary in order to obtain any sample at all (Willard 1989). Intestinal mucosa collected with sterile biopsy forceps, or fluid specimens collected with a sterile, guarded endoscopic sampling brush might provide superior samples for culture. The number and type of bacteria isolated could also have been influenced by variations in endoscope position within the alimentary tract. Radiographic determination of the position of the

insertion tube tip and the aspiration catheter at the time of sampling would help to confirm objectively a consistent location.

The bacteria isolated from the small intestinal fluid of healthy cats, using an endoscopic technique, was similar to those isolated from humans (Justesen and others 1984). Clostridium species are not usually isolated from the small intestinal fluid of humans (Justesen and others 1984) and a Clostridium species was isolated from only one healthy cat in this study. In an earlier study of young kittens, Clostridium species were isolated from the small intestine at post mortem examination (Williams Smith 1965). Recently, small intestinal bacterial overgrowth and enhanced intestinal permeability have been described in healthy beagles (Batt and others 1992) and this finding might also account for the large numbers of bacteria isolated from the small intestinal fluid specimens of some healthy cats in the present study. However, specimen contamination during collection seems a more likely explanation, because carbohydrate malassimilation was not demonstrated in the healthy cats by measurement of breath hydrogen excretion.

Small intestinal bacterial overgrowth has been defined principally by bacterial numbers (>lo5 or >lo6 cfu/ml bacteria, and including coliforms and anaerobes) (King and Toskes 1979, Batt and others 1983, Corazza and others 1990) and bacterial species and numbers have been correlated with biochemical damage to the mucosa in dogs (Batt and others 1983, 1988). In this study, increased numbers of Clostridium species were isolated from the cats with carbohydrate malassimilation, compared with the healthy cats. Anaerobes, and Clostridium species in particular, have been implicated in small intestinal bacterial overgrowth and enteropathies in dogs (Batt and others 1983, 1988, Kruth and others 1989). Further study is required to examine whether mucosal injury is associated with the presence of such bacteria in cats. Biochemical mucosal damage can occur in dogs with small intestinal bacterial overgrowth, without associated in- flammation (Batt and McLean 1987) and this may be one explanation why inflammatory bowel disease was not seen histopathologically in all the cats with chronic diarrhoea and, or, vomiting.

Measurement of breath hydrogen excretion after oral administration of carbohydrate to cats may be a simple non-invasive test for detecting carbohydrate malassimilation associated with an abnormal small intestinal bacterial flora. The test is easy to perform and may provide a useful indi- cation for endoscopy. Further study is necessary to determine whether endoscopy can provide a reproducible, reliable method for the collection of small intestinal fluid specimens in cats.

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ACKNOWLEDGEMENTS The assistance of the veterinarians who

referred these cats to the Feline Centre is grate- fully acknowledged.

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66, 110-113

~010gy69, 111-115

WASHABAU, R. J., STROMBECK, D. R., BUFFINGTON, C. A. & HAR-

1402-1406

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Breath hydrogen excretion after oral administration of xylose to cats